Plastic Corollary Discharge Predicts Sensory Consequences of Movements in a Cerebellum-Like Circuit

Abstract

SUMMARY The capacity to predict the sensory consequences of movements is critical for sensory, motor, and cognitive function. Though it is hypothesized that internal signals related to motor commands, known as corollary discharge, serve to generate such predictions, this process remains poorly understood at the neural circuit level. Here we demonstrate that neurons in the electrosensory lobe (ELL) of weakly electric mormyrid fish generate negative images of the sensory consequences of the fish’s own movements based on ascending spinal corollary discharge signals. These results generalize previous findings describing mechanisms for generating negative images of the effects of the fish’s specialized electric organ discharge (EOD) and suggest that a cerebellum-like circuit endowed with associative synaptic plasticity acting on corollary discharge can solve the complex and ubiquitous problem of predicting sensory consequences of movements.

Sustained sensorimotor control as intermittent decisions about prediction errors: computational framework and application to ground vehicle steering

“…It will be shown how a prediction signal that is useful in the intermittent control context can be generated similarly to the intermittent control itself: as a superposition of simple primitives. Neuronal recordings from animals show time histories of corollary discharge biases that follow a general pattern of rapid initial increase followed by slower decay (Poulet and Hedwig 2007; Chagnaud and Bass 2013; Requarth and Sawtell 2014); interestingly the near-optimal “prediction primitives” proposed here for intermittent sensorimotor control take a similar form.…”

A comparative approach to cerebellar function: insights from electrosensory systems

“…However, one question has been whether mechanisms for predicting the sensory consequences of motor commands related to simple, highly stereotyped behavior like the EOD are sufficient to solve the more complex problem of predicting the sensory consequences of motor commands for movements. Recent studies of mormyrid fish addressed this issue by demonstrating that in addition to corollary discharge signals related to the EOD, mossy fibers in mormyrid fish also convey a rich set of skeletomotor corollary discharge signals related to the fish’s swimming movements[58;59]. ELL neurons were shown to be capable of simultaneously generating and storing two opposite negative images related to different movement commands, i.e.…”

Skilled forelimb movements and internal copy motor circuits

“…Indeed, recent studies clarify roles for spinal copy pathways in filtering the sensory consequences of swimming movements in teleosts [56], and stabilizing ocular movements during locomotion in Xenopus [57]. From evolutionarily old origins, spinal internal copy pathways have presumably emerged and expanded in concert with the elaboration of mammalian limb movements.…”